- Email: [email protected]
Who rises to the challenge? Testing the Challenge Hypothesis in fish, amphibians, reptiles, and mammals
Hormones and Behavior xxx (xxxx) xxx–xxx
Contents lists available at ScienceDirect
Hormones and Behavior journal homepage: www.elsevier.com/locate/yhbeh
Review article
Who rises to the challenge? Testing the Challenge Hypothesis in fish, amphibians, reptiles, and mammals ⁎
Ignacio T. Moorea, , Jessica Hernandeza, Wolfgang Goymannb a b
2119 Derring Hall, Department of Biological Sciences, Virginia Tech, Blacksburg, VA 24061-0406, USA Abteilung für Verhaltensneurobiologie, Max-Planck-Institut für Ornithologie, Eberhard-Gwinner-Str. 6a, D-82319 Seewiesen, Germany
A R T I C LE I N FO
A B S T R A C T
Keywords: Challenge Hypothesis Testosterone Mating system Simulated territorial intrusion Androgens
According to the Challenge Hypothesis, social interactions, particularly among males, have a strong influence on circulating androgen levels. Specifically, males should respond to social challenges from conspecific males with a rapid increase in plasma androgen levels which support and stimulate further aggression. This basic tenet of the Challenge Hypothesis, an androgen increase in response to a social challenge from another male, has been tested in all vertebrate classes. While early studies generally supported the Challenge Hypothesis, more recent work has noted numerous exceptions, particularly in birds. Here, we conduct a meta-analysis of studies in fish, amphibians, non-avian reptiles, and mammals that test the prediction that circulating androgen levels of males should increase in response to an experimental challenge from another male. We found that teleost fish often increase androgens during such challenges, but other vertebrate groups show more mixed results. Why should fish be different from the other taxa? In fish with paternal care of young, the potential conflict between mating, being aggressive towards other males, and taking care of offspring is alleviated, because females typically choose males based on their defense of an already existing nest. Hence, rather than regulating the trade-off between mating, aggression, and parenting, androgens may have been co-opted to promote all three behaviors. For other taxa, increasing androgen levels only makes sense when the increase directly enhances reproductive success. Thus, the increase in androgen levels is a response to mating opportunities rather than a response to challenge from another male. To further our understanding of the role of a change in androgen levels in mediating behavioral decision-making between mating, aggression, and parenting, we need studies that address the behavioral consequences of an increase in androgens after male-male encounters and studies that test the androgen responsiveness of species that differ in the degree of paternal care.
1. Introduction The Challenge Hypothesis (Wingfield et al., 1990) was originally formulated to explain seasonal changes in plasma androgen levels (typically testosterone) in male birds as well as to predict how androgen levels would respond to social challenges, primarily from rival males. While earlier studies suggested that androgen levels would simply be elevated during the breeding season, studies of free-living birds had shown androgen levels to be much more dynamic, with levels rising above what is necessary for reproductive activity (Soma, 2006; Wingfield and Farner, 1978a; Wingfield and Farner, 1978b; Wingfield and Grimm, 1977). In light of these insights, predictions based on the Challenge Hypothesis suggested that social interactions were key mediators of plasma androgen levels, with male-male competition being the most prominent factor. As such, androgen levels were
⁎
predicted to be highest during the period when males compete for access to mates. While Wingfield and colleagues (Wingfield et al., 1987; Wingfield et al., 1990) initially aimed to explain the variation in androgen levels of birds, other researchers quickly adopted the idea to explain individual-, population-, and species-level variation in androgen levels within other vertebrate groups, including humans (e.g. Archer, 2006; Hirschenhauser and Oliveira, 2006; Hirschenhauser et al., 2004; Hirschenhauser et al., 2003). Indeed, similar seasonal patterns of androgen levels (highest levels early in the breeding season when males compete for access to mates) have been described in many seasonally reproducing male vertebrates. Social mating system and the degree of care that the male provides are two other factors that affect plasma androgen levels as well as the androgen response to a social challenge (Wingfield et al., 1990). Males of monogamous and polyandrous species should express a high
Corresponding author. E-mail address: [email protected] (I.T. Moore).
https://doi.org/10.1016/j.yhbeh.2019.06.001 Received 1 May 2019; Received in revised form 31 May 2019; Accepted 5 June 2019 0018-506X/ © 2019 Elsevier Inc. All rights reserved.
Please cite this article as: Ignacio T. Moore, Jessica Hernandez and Wolfgang Goymann, Hormones and Behavior, https://doi.org/10.1016/j.yhbeh.2019.06.001
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males and male contributions to care should be less drastic than in birds. Making proper predictions for changes in androgen levels during male-male interactions becomes even more challenging for species such as the California mouse (Peromyscus californicus) in which it has been demonstrated that testosterone promotes paternal care (Trainor and Marler, 2002). For California mice it seems as if testosterone has been co-opted for caring decisions and – unlike in birds – does not seem to be involved in regulating the trade-off between mating and parenting. In combination, though, increasing androgen levels during male-male encounters should be less costly for male mammals than male birds and hence, one would predict that male-male encounters could lead to an increase in androgen levels during male-male interactions if this should help males to prepare for future encounters. As with most mammals, males of non-avian reptiles should maintain high plasma androgen levels as long as fertile females are available. To our knowledge, there are no non-avian reptile species in which males provide parental care (Reynolds et al., 2002). As a consequence, elevating androgen levels during male-male interactions should not be associated with paternal care costs. Hence, if the variation in androgen levels among individuals during the breeding season is mainly a function of aggressive interactions among males, then males should elevate androgen levels during simulated territorial intrusions. For fish, the situation is complicated as their mating systems and degrees of paternal care are highly variable and dynamic. The majority of fish species do not provide parental care, but all species that have been experimentally tested during male-male interactions belong to species in which either males, females, or both parents, provide offspring care. However, even in these species in which males provide offspring care, a trade-off between mating and parenting should be absent or relaxed, because females typically prefer to spawn with males that already tend a nest (Coleman and Jones, 2011; Forsgren et al., 1996; Kahn et al., 2013), and tending a nest often involves defending it from marauding males. Thus, fish should typically be able to elevate plasma androgen levels during conflicts with other males without experiencing a cost to parental care.
androgen responsiveness, which means they should express high levels of androgens primarily during the period of territory establishment and when their female mates are fertile. At other times, and in particular during paternal care of young, androgen levels should be low, but quickly rise when challenged by other males. In contrast, males of polygynous species should maintain elevated androgen levels as long as there are fertile females in the population and thus have low androgen responsiveness. In other words, with such prolonged periods (length of the breeding season) of elevated levels of androgens, males show limited capacities to further elevate them when challenged by other males. Finally, observational studies show lowest androgen levels in males that care for young and experimental studies show that elevating male plasma androgen levels interferes with care (often feeding) of young (reviewed by Lynn et al., 2009; Wingfield et al., 2001). One of the prime predictions from the Challenge Hypothesis is that androgen levels are responsive to social interactions, primarily competition between males. Indeed, the origins of the Challenge Hypothesis were the observations that androgens in male birds peak during periods of intense competition for mates and territories (Wingfield and Farner, 1978a; Wingfield and Farner, 1978b). Thus, androgen levels above breeding baseline are thought to have enhancing effects on male-male aggression and/or mate guarding. One of the basic experimental tests of the Challenge Hypothesis is based on the prediction that androgen levels in males should increase in response to a challenge from another male (e.g. Wingfield and Wada, 1989). In such an experiment, a captive or taxidermic mount of a male is introduced onto the territory of the focal male and the behavioral and androgen response is quantified. While early studies were supportive (as are broader observational seasonal patterns of androgen levels), experimental evidence in birds has shown that the androgen response to male-male challenges is inconsistent. We have recently conducted a meta-analysis on all simulated territorial intrusion studies on birds and have found limited experimental support for the prediction that male-male challenges should lead to elevated androgen levels (Goymann et al., 2019). In contrast, most studies are consistent with the idea that social interactions with fertile females induce an increase in plasma androgen levels in male birds. We have thus modified the predictions and suggested a Challenge Hypothesis 2.0 that makes male-female interactions the focus of acute changes in males' androgen levels. In addition, we extended the modified predictions to other vertebrate taxa. Experimental tests of the Challenge Hypothesis have also been conducted in fish, amphibians, non-avian reptiles, and mammals, but these groups have not received as much attention as birds. In the current study, we apply the approach that we have previously used on birds (Goymann et al., 2019) to these other taxa, focusing on the question: do plasma androgen levels increase in males in response to a conspecific territorial intrusion from another male? In other words, we have focused the current meta-analysis on experimental tests of the Challenge Hypothesis rather than observational studies describing seasonal hormone patterns (for observational study see: Hirschenhauser et al., 2003). For each group of animals, we derived specific predictions that are based on their naturaland life-histories (see also Table 1 in Goymann et al., 2019). In most mammals, males do not contribute substantially to parental care. Thus, if interactions with females are the main drivers of variation in male androgen levels, then males should maintain high androgen levels as long as fertile females are around. Further, because there is no trade-off between mating and parenting, male mammals could further elevate plasma androgen levels during male-male encounters. Predicting the outcome for male-male interactions becomes more complicated for mammals in which males assist females in caring for young. Analogous to birds, caring males should not elevate androgen levels if those levels suppress paternal care. However, paternal contributions to offspring care in mammals rarely reach the degree of care seen in male birds and the fitness consequences of an absence of care may not be as impactful in male mammals as they may be in birds. Hence, a potential trade-off between aggression towards conspecific
2. Methods In December 2018 we searched the Web of Science for all articles that cited the original Challenge Hypothesis by Wingfield and colleagues (1376 citations) and selected all studies that used experimental approaches to study the effect of male-male encounters on plasma androgen levels in fish, amphibians, non-avian reptiles, and mammals (11-ketotestosterone and testosterone in fish, and testosterone in the other groups). We first tried to restrict the analysis to experimental territorial intrusion studies (often called simulated territorial intrusions) conducted in free-living animals, but this was not possible, since only one out of a total of nine publications on eight mammalian species and two out of 14 publications on 14 fish species were conducted in free-living individuals. Therefore, we included the captive studies in our comparison. For non-avian reptiles, we selected seven comparisons of free-living animals (four publications) that came from only three species. For amphibians we found only one study. See figures for list of species included and references. From these studies we extracted the mean plasma androgen concentration of challenged versus control animals, the respective standard errors, and sample sizes. From these androgen data we calculated the standardized effect sizes and their 95% confidence intervals. Standardized effect sizes are defined as the difference between two means divided by the pooled standard deviation for those means (Cohen, 1990) and, in the case of this study, represent a measure of the magnitude of the difference in androgen levels between control and challenged individuals on a standardized scale. Thus, they allow a direct comparison of the magnitude of a response independent of absolute differences in the respective measurements. Standardized effect sizes and their 95% confidence intervals were calculated using the program ESCIdelta (Cumming and Finch, 2001). 2
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Fig. 1. Meta-analysis of simulated territorial intrusion experiments in fish. Effect sizes (and 95% confidence limits) of the change in (A) 11-ketotestosterone concentrations and (B) testosterone during simulated territorial intrusions (STI) compared to control situations of male birds. The red dotted vertical line indicates no difference in testosterone concentrations between STI and control males. A negative effect size means that testosterone concentrations were lower after STIs than in controls while a positive effect size indicates an increase in testosterone after STIs compared to controls. If the 95% confidence limits of the effect size cross the red dotted line, the STI treatment did not lead to a significant change in testosterone concentrations.
3. Results
10 of these the 95% confidence interval did not cross zero, suggesting that there was a positive effect of male-male interactions (Fig. 1A). Similarly, for testosterone all 13 tests had a positive effect size and in seven of these the 95% confidence intervals did not cross zero,
For 11-ketotestosterone in teleost fish, 16 of 20 tests had a positive effect size (the other four were either zero or slightly negative) and in 3
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Fig. 2. Effect sizes of the change in testosterone during simulated territorial intrusion experiments in non-avian reptiles (see Fig. 1 for details).
non-avian reptiles (with the caveat that only three, closely related species were tested), and the only tested amphibian were close to zero, rendering no broad support for the prediction that male-male encounters lead to an increase in circulating androgen levels in these taxa. There are a number of possible explanations for the lack of support for the social challenge aspect of the Challenge Hypothesis. First, it is worth noting that a simple positive relationship between androgens and aggression is not universal because aggression has multiple forms (Moyer, 1968). For example, aggression that results in increased reproductive opportunities is more likely to be positively associated with androgens than is aggression that serves more of a survival or defensive role (Adkins-Regan, 2005). A few other alternative hypotheses have been proposed, primarily in studies of birds, to explain the lack of support for the Challenge Hypothesis (Goymann et al., 2007; Landys et al., 2007; Lynn, 2008; Wingfield and Hunt, 2002). For example, previous reviews of primarily observational studies identified paternal care to be a key contributor to variation in plasma androgen levels (Hirschenhauser and Oliveira, 2006; Hirschenhauser et al., 2003). Indeed, with a few exceptions, paternal care of young is negatively associated with circulating androgen levels (Lynn, 2016). A more recent proposal is that male-female interactions are more important for mediating an androgen response than male-male interactions. As such, there is considerable evidence that male birds elevate plasma androgen levels in response to cues from fertile females, which led us to propose a modified Challenge Hypothesis 2.0 (Goymann et al., 2019). Given the enduring influence of the Challenge Hypothesis (cited over 500 times in the last 5 years alone according to Google Scholar), why do we not see consistent support but rather a diversity of results from experimental tests? One key explanatory variable (that needs further attention) may be paternal care, specifically the degree to which there is a trade-off between paternal care and responding to a conspecific territorial challenge. For many animals, such as birds, there is a distinct trade-off between paternal care of young and responding to a
suggesting an overall positive effect of male-male encounters on testosterone levels (Fig. 1B). The only tested amphibian, the Smith tree frog (Hypsiboas faber) had a negative effect size (Cohen's d = −0.192 ± 0.816) and did not elevate testosterone during male-male interactions. In the three tested species of non-avian reptiles, six of 12 comparisons showed positive effect sizes, but all effect sizes were close to zero (seven of the 12 comparisons referred to testosterone levels at different time points after the challenge in one species; Fig. 2). In mammals, 10 of 12 comparisons showed positive effect sizes (Fig. 3). However, only subordinate greater long-tailed hamsters (Tscheskia triton) and California mice (Peromyscus californicus) had a 95% confidence interval that did not cross zero and thus showed a consistent and significant rise in testosterone (or in fecal testosterone metabolites) after experimental encounters with other males.
4. Discussion Perhaps one of the most basic and tested tenets of the Challenge Hypothesis is that plasma androgen levels should increase in response to a social challenge from another male. In a previous study we tested this prediction in birds and found only limited support, suggesting that males of most species of birds do not elevate plasma androgen levels during male-male interactions (Goymann et al., 2019). Here, we extend the meta-analysis of the effect of male-male encounters on androgen levels to fish, amphibians, non-avian reptiles, and (non-human) mammals. As with birds, we document an inconsistent pattern across these other taxa. Within fish there was relatively broad support for an increase in plasma androgen levels in response to an experimental territorial challenge. That is, most fish showed a positive effect size with challenged males expressing higher testosterone and/or 11-ketotestosterone than controls, and the effect sizes were significantly positive in a good number of studies. However, the effect sizes in most mammals, all 4
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Fig. 3. Effect sizes of the change in testosterone during simulated territorial intrusion experiments in mammals (see Fig. 1 for details).
much more keenly responsive to the reproductive status of their mate and in which paternity is known. We would predict those truly monogamous males to be more responsive to female copulation solicitations than to male challenges. Further, the Challenge Hypothesis has not been tested in socially polygynous species such as those that exhibit lektype breeding systems. In those systems, males provide no paternal care of young, so there should be no trade-off between responding to a challenge and caring for young. Second, future studies should investigate male responses to interactions with females and these should be done across a wide variety of species. As we have recently proposed (Goymann et al., 2019), there is reason to believe that the opportunity for immediate reproductive success may be more important for mediating an androgen response than a challenge from another male that has only indirect possible reproductive benefits. Third, hormonal studies on the winner-and-loser effect suggest that androgens may be involved in mediating this effect (albeit the effects seem to substantially differ between taxa, e.g. Fuxjager et al., 2010; Fuxjager and Marler, 2010; Hirschenhauser et al., 2013; Oliveira et al., 2009). Currently, we lack an integration of the winner-and-loser paradigm with the Challenge Hypothesis [(see: Apfelbeck et al., 2011 for an attempt) and (Goymann et al., 2007; Kempenaers et al., 2008 for more detailed discussion)]. A rise in testosterone during male-male challenges has been suggested to increase the persistence of aggression and prepare the contestant for future encounters with other rivals, but experimental evidence for this, particularly in a field setting, is still limited [(Wingfield, 1994) (but see Goymann et al., 2015)]. In general, the incorporation of psychological studies (both human and rodent) into the eco-physiological realm would be productive. As our understanding of the neuroendocrine mechanisms and the context of aggression has been broadened (Eisenegger et al., 2011), their investigation in freeliving animals will further show if and how androgens mediate aggression. Most importantly, further conceptual contributions and experimental studies to elucidate the potential ecological and
male challenge as androgens suppress the former while they promote the latter. In such cases, responding to a conspecific challenge by elevating androgen levels would potentially have immediate negative effects on paternal care and thus fitness (e.g. Goymann and Dávila, 2017). However, for some animals including many fish, there is no trade-off between paternal care and responding to a conspecific territorial challenge. For fish, paternal care often means defending a nest site from competitors and predators as well as aerating the eggs. The same nest defense behavior also serves males to attract additional mates because females typically prefer to spawn with males that already have a nest with eggs (Coleman and Jones, 2011; Forsgren et al., 1996; Kahn et al., 2013). In those cases, there is no trade-off between mating effort and paternal care for androgens to mediate and thus androgens could have been co-opted to foster both kinds of behaviors. An increase in androgens could serve aggression and nest-tending at the same time with no associated costs in terms of parenting. Future studies should focus on a few distinct questions to try to understand variability in plasma androgen levels. First and foremost, a broader and more even distribution of sampling across the vertebrate classes is warranted. For example, we currently only have a single experimental study of an amphibian and yet amphibians offer a great variety of life-history traits and behaviors that are associated with androgens including paternal care, female mate choice, and male-male competition. Fish are another group with great variability in life-history traits associated with androgens. Focused studies on particular taxa, such as amphibians and fish that express a large variety in the degree of paternal care or mating system, are likely to provide important results from which broader conclusions can be made. Even within birds, the best studied group in terms of the Challenge Hypothesis, the majority of studies come from passerines with relatively similar life histories. The vast majority of passerines are socially monogamous but genetically polygynous. It could prove enlightening to test the Challenge Hypothesis in truly monogamous species in which males should be 5
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evolutionary benefits (and costs) of acute changes in androgen levels during social encounters are urgently needed.
Hirschenhauser, K., Taborsky, M., Oliveira, A.V., Canàrio, A.V.M., Oliveira, R.F., 2004. A test of the 'challenge hypothesis' in cichlid fish: simulated partner and territory intruder experiments. Anim. Behav. 68, 741–750. Hirschenhauser, K., Gahr, M., Goymann, W., 2013. Winning and losing in public: audiences direct future success in Japanese quail. Horm. Behav. 63, 625–633. Kahn, A.T., Schwanz, L.E., Kokko, H., 2013. Paternity protection can provide a kick-start for the evolution of male-only parental care. Evolution 67, 2207–2217. Kempenaers, B., Peters, A., Foerster, K., 2008. Sources of individual variation in plasma testosterone levels. Philos. Trans. R. Soc., B 363, 1711–1723. Landys, M.M., Goymann, W., Raess, M., Slagsvold, T., 2007. Hormonal responses to malemale social challenge in the blue tit Cyanistes caeruleus: single broodedness as an explanatory variable. Physiol. Biochem. Zool. 80, 228–240. Lynn, S.E., 2008. Behavioral insensitivity to testosterone: why and how does testosterone alter paternal and aggressive behavior in some avian species but not others? Gen. Comp. Endocrinol. 157, 233–240. Lynn, S.E., 2016. Endocrine and neuroendocrine regulation of fathering behavior in birds. Horm. Behav. 77, 237–248. Lynn, S.E., Prince, L.E., Schook, D.M., Moore, I.T., 2009. Supplementary testosterone inhibits paternal care in a tropically breeding sparrow, Zonotrichia capensis. Physiol. Biochem. Zool. 82, 699–708. Moyer, K.E., 1968. Kinds of aggression and their physiological basis. Commun. Behav. Biol. 2, 65–87. Oliveira, R.F., Silva, A., Canario, A.V.M., 2009. Why do winners keep winning? Androgen mediation of winner but not loser effects in cichlid fish. Proc. R. Soc. B Biol. Sci. 276, 2249–2256. Reynolds, J.D., Goodwin, N.B., Freckleton, R.P., 2002. Evolutionary transitions in parental care and live bearing in vertebrates. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357, 269–281. Soma, K.K., 2006. Testosterone and aggression: Berthold, birds and beyond. J. Neuroendocrinol. 18, 543–551. Trainor, B.C., Marler, C.A., 2002. Testosterone promotes paternal behaviour in a monogamous mammal via conversion to oestrogen. Proc. R. Soc. B 269, 823–829. Wingfield, J.C., 1994. Regulation of territorial behavior in the sedentary song sparrow, Melospiza melodia morphna. Horm. Behav. 28, 1–15. Wingfield, J.C., Farner, D.S., 1978a. The annual cycle of plasma irLH and steroid hormones in feral populations of the white-crowned sparow, Zonotrichia leucophrys gambelii. Biol. Reprod. 19, 1046–1056. Wingfield, J.C., Farner, D.S., 1978b. The endocrinology of a natural breeding population of the white-crowned sparrow (Zonotrichia leucophrys pugetensis). Physiol. Zool. 51, 188–205. Wingfield, J.C., Grimm, A.S., 1977. Seasonal changes in plasma cortisol, testosterone and oestradiol-17Bin the plaice, Pleuronectes platessa L. Gen. Comp. Endocrinol. 31, 1–11. Wingfield, J.C., Hunt, K.E., 2002. Arctic spring: hormone-behavior interactions in a severe environment. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 132, 275–286. Wingfield, J.C., Wada, M., 1989. Changes in plasma levels of testosterone during malemale interactions in the song sparrow, Melospiza melodia: time course and specificity of response. J. Comp. Physiol. A. 166, 189–194. Wingfield, J.C., Ball, G.F., Dufty, A.M., Hegner, R.E., Ramenofsky, M., 1987. Testosterone and aggression in birds. Am. Sci. 75, 602–608. Wingfield, J.C., Hegner, R.E., Dufty, A.M., Ball, G.F., 1990. The "Challenge Hypothesis": theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nat. 136, 829–846. Wingfield, J.C., Lynn, S.E., Soma, K.K., 2001. Avoiding the 'costs' of testosterone: ecological bases of hormone-behavior interactions. Brain Behav. Evol. 57, 239–251.
Acknowledgements ITM acknowledges funding through NSF grant no. IOS-1353093. JH was supported by an NSF GRFP. WG was funded by the Max-PlanckGesellschaft. References Adkins-Regan, E., 2005. Hormones and Animal Social Behavior. Princeton University Press. Apfelbeck, B., Stegherr, J., Goymann, W., 2011. Simulating winning in the wild - the behavioral and hormonal response of black redstarts to single and repeated territorial challenges of high and low intensity. Horm. Behav. 60, 565–571. Archer, J., 2006. Testosterone and human aggression: an evaluation of the challenge hypothesis. Neurosci. Biobehav. Rev. 30, 319–345. Cohen, J., 1990. Things I have learned (so far). Am. Psychol. 45, 1304–1312. https://doi. org/10.1037/0003-066X.45.12.1304. Coleman, S.W., Jones, A.G., 2011. Patterns of multiple paternity and maternity in fishes. Biol. J. Linn. Soc. 103, 735–760. Cumming, G., Finch, S., 2001. A primer on the understanding, use, and calculation of confidence intervals that are based on central and non- central distributions. Educ. Psychol. Meas. 61, 532–574. https://doi.org/10.1177/0013164401614002. Eisenegger, C., Haushofer, J., Fehr, E., 2011. The role of testosterone in social interaction. Trends Cogn. Sci. 15, 263–271. Forsgren, E., Karlsson, A., Kvarnemo, C., 1996. Female sand gobies gain direct benefits by choosing males with eggs in their nests. Behav. Ecol. Sociobiol. 39, 91–96. Fuxjager, M.J., Marler, C.A., 2010. How and why the winner effect forms: influences of contest environment and species differences. Behav. Ecol. 21, 37–45. Fuxjager, M.J., Forbes-Lorman, R.M., Coss, D.J., Auger, C.J., Auger, A.P., Marler, C.A., 2010. Winning territorial disputes selectively enhances androgen sensitivity in neural pathways related to motivation and social aggression. Proc. Natl. Acad. Sci. 107, 12393–12398. Goymann, W., Dávila, P.F., 2017. Acute peaks of testosterone suppress paternal care: evidence from individual hormonal reaction norms. Proc. R. Soc. B Biol. Sci. 284, 20170632. Goymann, W., Landys, M.M., Wingfield, J.C., 2007. Distinguishing seasonal androgen responses from male-male androgen responsiveness - revisiting the challenge hypothesis. Horm. Behav. 51, 463–476. Goymann, W., Villavicencio, C.P., Apfelbeck, B., 2015. Does a short-term increase in testosterone affect the intensity or persistence of territorial aggression? - an approach using an individual's hormonal reactive scope to study hormonal effects on behavior. Physiol. Behav. 149, 310–316. Goymann, W., Moore, I.T., Oliveira, R.F., 2019. Challenge hypothesis 2.0: a fresh look at an established idea. BioScience 69 (6), 432–442. Hirschenhauser, K., Oliveira, R.F., 2006. Social modulation of androgens in male vertebrates: meta-analysis of the challenge hypothesis. Anim. Behav. 71, 265–277. Hirschenhauser, K., Winkler, H., Oliveira, R.F., 2003. Comparative analysis of male androgen responsiveness to social environment in birds: the effects of mating system and paternal incubation. Horm. Behav. 43, 508–519.
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Contents lists available at ScienceDirect
Hormones and Behavior journal homepage: www.elsevier.com/locate/yhbeh
Review article
Who rises to the challenge? Testing the Challenge Hypothesis in fish, amphibians, reptiles, and mammals ⁎
Ignacio T. Moorea, , Jessica Hernandeza, Wolfgang Goymannb a b
2119 Derring Hall, Department of Biological Sciences, Virginia Tech, Blacksburg, VA 24061-0406, USA Abteilung für Verhaltensneurobiologie, Max-Planck-Institut für Ornithologie, Eberhard-Gwinner-Str. 6a, D-82319 Seewiesen, Germany
A R T I C LE I N FO
A B S T R A C T
Keywords: Challenge Hypothesis Testosterone Mating system Simulated territorial intrusion Androgens
According to the Challenge Hypothesis, social interactions, particularly among males, have a strong influence on circulating androgen levels. Specifically, males should respond to social challenges from conspecific males with a rapid increase in plasma androgen levels which support and stimulate further aggression. This basic tenet of the Challenge Hypothesis, an androgen increase in response to a social challenge from another male, has been tested in all vertebrate classes. While early studies generally supported the Challenge Hypothesis, more recent work has noted numerous exceptions, particularly in birds. Here, we conduct a meta-analysis of studies in fish, amphibians, non-avian reptiles, and mammals that test the prediction that circulating androgen levels of males should increase in response to an experimental challenge from another male. We found that teleost fish often increase androgens during such challenges, but other vertebrate groups show more mixed results. Why should fish be different from the other taxa? In fish with paternal care of young, the potential conflict between mating, being aggressive towards other males, and taking care of offspring is alleviated, because females typically choose males based on their defense of an already existing nest. Hence, rather than regulating the trade-off between mating, aggression, and parenting, androgens may have been co-opted to promote all three behaviors. For other taxa, increasing androgen levels only makes sense when the increase directly enhances reproductive success. Thus, the increase in androgen levels is a response to mating opportunities rather than a response to challenge from another male. To further our understanding of the role of a change in androgen levels in mediating behavioral decision-making between mating, aggression, and parenting, we need studies that address the behavioral consequences of an increase in androgens after male-male encounters and studies that test the androgen responsiveness of species that differ in the degree of paternal care.
1. Introduction The Challenge Hypothesis (Wingfield et al., 1990) was originally formulated to explain seasonal changes in plasma androgen levels (typically testosterone) in male birds as well as to predict how androgen levels would respond to social challenges, primarily from rival males. While earlier studies suggested that androgen levels would simply be elevated during the breeding season, studies of free-living birds had shown androgen levels to be much more dynamic, with levels rising above what is necessary for reproductive activity (Soma, 2006; Wingfield and Farner, 1978a; Wingfield and Farner, 1978b; Wingfield and Grimm, 1977). In light of these insights, predictions based on the Challenge Hypothesis suggested that social interactions were key mediators of plasma androgen levels, with male-male competition being the most prominent factor. As such, androgen levels were
⁎
predicted to be highest during the period when males compete for access to mates. While Wingfield and colleagues (Wingfield et al., 1987; Wingfield et al., 1990) initially aimed to explain the variation in androgen levels of birds, other researchers quickly adopted the idea to explain individual-, population-, and species-level variation in androgen levels within other vertebrate groups, including humans (e.g. Archer, 2006; Hirschenhauser and Oliveira, 2006; Hirschenhauser et al., 2004; Hirschenhauser et al., 2003). Indeed, similar seasonal patterns of androgen levels (highest levels early in the breeding season when males compete for access to mates) have been described in many seasonally reproducing male vertebrates. Social mating system and the degree of care that the male provides are two other factors that affect plasma androgen levels as well as the androgen response to a social challenge (Wingfield et al., 1990). Males of monogamous and polyandrous species should express a high
Corresponding author. E-mail address: [email protected] (I.T. Moore).
https://doi.org/10.1016/j.yhbeh.2019.06.001 Received 1 May 2019; Received in revised form 31 May 2019; Accepted 5 June 2019 0018-506X/ © 2019 Elsevier Inc. All rights reserved.
Please cite this article as: Ignacio T. Moore, Jessica Hernandez and Wolfgang Goymann, Hormones and Behavior, https://doi.org/10.1016/j.yhbeh.2019.06.001
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males and male contributions to care should be less drastic than in birds. Making proper predictions for changes in androgen levels during male-male interactions becomes even more challenging for species such as the California mouse (Peromyscus californicus) in which it has been demonstrated that testosterone promotes paternal care (Trainor and Marler, 2002). For California mice it seems as if testosterone has been co-opted for caring decisions and – unlike in birds – does not seem to be involved in regulating the trade-off between mating and parenting. In combination, though, increasing androgen levels during male-male encounters should be less costly for male mammals than male birds and hence, one would predict that male-male encounters could lead to an increase in androgen levels during male-male interactions if this should help males to prepare for future encounters. As with most mammals, males of non-avian reptiles should maintain high plasma androgen levels as long as fertile females are available. To our knowledge, there are no non-avian reptile species in which males provide parental care (Reynolds et al., 2002). As a consequence, elevating androgen levels during male-male interactions should not be associated with paternal care costs. Hence, if the variation in androgen levels among individuals during the breeding season is mainly a function of aggressive interactions among males, then males should elevate androgen levels during simulated territorial intrusions. For fish, the situation is complicated as their mating systems and degrees of paternal care are highly variable and dynamic. The majority of fish species do not provide parental care, but all species that have been experimentally tested during male-male interactions belong to species in which either males, females, or both parents, provide offspring care. However, even in these species in which males provide offspring care, a trade-off between mating and parenting should be absent or relaxed, because females typically prefer to spawn with males that already tend a nest (Coleman and Jones, 2011; Forsgren et al., 1996; Kahn et al., 2013), and tending a nest often involves defending it from marauding males. Thus, fish should typically be able to elevate plasma androgen levels during conflicts with other males without experiencing a cost to parental care.
androgen responsiveness, which means they should express high levels of androgens primarily during the period of territory establishment and when their female mates are fertile. At other times, and in particular during paternal care of young, androgen levels should be low, but quickly rise when challenged by other males. In contrast, males of polygynous species should maintain elevated androgen levels as long as there are fertile females in the population and thus have low androgen responsiveness. In other words, with such prolonged periods (length of the breeding season) of elevated levels of androgens, males show limited capacities to further elevate them when challenged by other males. Finally, observational studies show lowest androgen levels in males that care for young and experimental studies show that elevating male plasma androgen levels interferes with care (often feeding) of young (reviewed by Lynn et al., 2009; Wingfield et al., 2001). One of the prime predictions from the Challenge Hypothesis is that androgen levels are responsive to social interactions, primarily competition between males. Indeed, the origins of the Challenge Hypothesis were the observations that androgens in male birds peak during periods of intense competition for mates and territories (Wingfield and Farner, 1978a; Wingfield and Farner, 1978b). Thus, androgen levels above breeding baseline are thought to have enhancing effects on male-male aggression and/or mate guarding. One of the basic experimental tests of the Challenge Hypothesis is based on the prediction that androgen levels in males should increase in response to a challenge from another male (e.g. Wingfield and Wada, 1989). In such an experiment, a captive or taxidermic mount of a male is introduced onto the territory of the focal male and the behavioral and androgen response is quantified. While early studies were supportive (as are broader observational seasonal patterns of androgen levels), experimental evidence in birds has shown that the androgen response to male-male challenges is inconsistent. We have recently conducted a meta-analysis on all simulated territorial intrusion studies on birds and have found limited experimental support for the prediction that male-male challenges should lead to elevated androgen levels (Goymann et al., 2019). In contrast, most studies are consistent with the idea that social interactions with fertile females induce an increase in plasma androgen levels in male birds. We have thus modified the predictions and suggested a Challenge Hypothesis 2.0 that makes male-female interactions the focus of acute changes in males' androgen levels. In addition, we extended the modified predictions to other vertebrate taxa. Experimental tests of the Challenge Hypothesis have also been conducted in fish, amphibians, non-avian reptiles, and mammals, but these groups have not received as much attention as birds. In the current study, we apply the approach that we have previously used on birds (Goymann et al., 2019) to these other taxa, focusing on the question: do plasma androgen levels increase in males in response to a conspecific territorial intrusion from another male? In other words, we have focused the current meta-analysis on experimental tests of the Challenge Hypothesis rather than observational studies describing seasonal hormone patterns (for observational study see: Hirschenhauser et al., 2003). For each group of animals, we derived specific predictions that are based on their naturaland life-histories (see also Table 1 in Goymann et al., 2019). In most mammals, males do not contribute substantially to parental care. Thus, if interactions with females are the main drivers of variation in male androgen levels, then males should maintain high androgen levels as long as fertile females are around. Further, because there is no trade-off between mating and parenting, male mammals could further elevate plasma androgen levels during male-male encounters. Predicting the outcome for male-male interactions becomes more complicated for mammals in which males assist females in caring for young. Analogous to birds, caring males should not elevate androgen levels if those levels suppress paternal care. However, paternal contributions to offspring care in mammals rarely reach the degree of care seen in male birds and the fitness consequences of an absence of care may not be as impactful in male mammals as they may be in birds. Hence, a potential trade-off between aggression towards conspecific
2. Methods In December 2018 we searched the Web of Science for all articles that cited the original Challenge Hypothesis by Wingfield and colleagues (1376 citations) and selected all studies that used experimental approaches to study the effect of male-male encounters on plasma androgen levels in fish, amphibians, non-avian reptiles, and mammals (11-ketotestosterone and testosterone in fish, and testosterone in the other groups). We first tried to restrict the analysis to experimental territorial intrusion studies (often called simulated territorial intrusions) conducted in free-living animals, but this was not possible, since only one out of a total of nine publications on eight mammalian species and two out of 14 publications on 14 fish species were conducted in free-living individuals. Therefore, we included the captive studies in our comparison. For non-avian reptiles, we selected seven comparisons of free-living animals (four publications) that came from only three species. For amphibians we found only one study. See figures for list of species included and references. From these studies we extracted the mean plasma androgen concentration of challenged versus control animals, the respective standard errors, and sample sizes. From these androgen data we calculated the standardized effect sizes and their 95% confidence intervals. Standardized effect sizes are defined as the difference between two means divided by the pooled standard deviation for those means (Cohen, 1990) and, in the case of this study, represent a measure of the magnitude of the difference in androgen levels between control and challenged individuals on a standardized scale. Thus, they allow a direct comparison of the magnitude of a response independent of absolute differences in the respective measurements. Standardized effect sizes and their 95% confidence intervals were calculated using the program ESCIdelta (Cumming and Finch, 2001). 2
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Fig. 1. Meta-analysis of simulated territorial intrusion experiments in fish. Effect sizes (and 95% confidence limits) of the change in (A) 11-ketotestosterone concentrations and (B) testosterone during simulated territorial intrusions (STI) compared to control situations of male birds. The red dotted vertical line indicates no difference in testosterone concentrations between STI and control males. A negative effect size means that testosterone concentrations were lower after STIs than in controls while a positive effect size indicates an increase in testosterone after STIs compared to controls. If the 95% confidence limits of the effect size cross the red dotted line, the STI treatment did not lead to a significant change in testosterone concentrations.
3. Results
10 of these the 95% confidence interval did not cross zero, suggesting that there was a positive effect of male-male interactions (Fig. 1A). Similarly, for testosterone all 13 tests had a positive effect size and in seven of these the 95% confidence intervals did not cross zero,
For 11-ketotestosterone in teleost fish, 16 of 20 tests had a positive effect size (the other four were either zero or slightly negative) and in 3
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Fig. 2. Effect sizes of the change in testosterone during simulated territorial intrusion experiments in non-avian reptiles (see Fig. 1 for details).
non-avian reptiles (with the caveat that only three, closely related species were tested), and the only tested amphibian were close to zero, rendering no broad support for the prediction that male-male encounters lead to an increase in circulating androgen levels in these taxa. There are a number of possible explanations for the lack of support for the social challenge aspect of the Challenge Hypothesis. First, it is worth noting that a simple positive relationship between androgens and aggression is not universal because aggression has multiple forms (Moyer, 1968). For example, aggression that results in increased reproductive opportunities is more likely to be positively associated with androgens than is aggression that serves more of a survival or defensive role (Adkins-Regan, 2005). A few other alternative hypotheses have been proposed, primarily in studies of birds, to explain the lack of support for the Challenge Hypothesis (Goymann et al., 2007; Landys et al., 2007; Lynn, 2008; Wingfield and Hunt, 2002). For example, previous reviews of primarily observational studies identified paternal care to be a key contributor to variation in plasma androgen levels (Hirschenhauser and Oliveira, 2006; Hirschenhauser et al., 2003). Indeed, with a few exceptions, paternal care of young is negatively associated with circulating androgen levels (Lynn, 2016). A more recent proposal is that male-female interactions are more important for mediating an androgen response than male-male interactions. As such, there is considerable evidence that male birds elevate plasma androgen levels in response to cues from fertile females, which led us to propose a modified Challenge Hypothesis 2.0 (Goymann et al., 2019). Given the enduring influence of the Challenge Hypothesis (cited over 500 times in the last 5 years alone according to Google Scholar), why do we not see consistent support but rather a diversity of results from experimental tests? One key explanatory variable (that needs further attention) may be paternal care, specifically the degree to which there is a trade-off between paternal care and responding to a conspecific territorial challenge. For many animals, such as birds, there is a distinct trade-off between paternal care of young and responding to a
suggesting an overall positive effect of male-male encounters on testosterone levels (Fig. 1B). The only tested amphibian, the Smith tree frog (Hypsiboas faber) had a negative effect size (Cohen's d = −0.192 ± 0.816) and did not elevate testosterone during male-male interactions. In the three tested species of non-avian reptiles, six of 12 comparisons showed positive effect sizes, but all effect sizes were close to zero (seven of the 12 comparisons referred to testosterone levels at different time points after the challenge in one species; Fig. 2). In mammals, 10 of 12 comparisons showed positive effect sizes (Fig. 3). However, only subordinate greater long-tailed hamsters (Tscheskia triton) and California mice (Peromyscus californicus) had a 95% confidence interval that did not cross zero and thus showed a consistent and significant rise in testosterone (or in fecal testosterone metabolites) after experimental encounters with other males.
4. Discussion Perhaps one of the most basic and tested tenets of the Challenge Hypothesis is that plasma androgen levels should increase in response to a social challenge from another male. In a previous study we tested this prediction in birds and found only limited support, suggesting that males of most species of birds do not elevate plasma androgen levels during male-male interactions (Goymann et al., 2019). Here, we extend the meta-analysis of the effect of male-male encounters on androgen levels to fish, amphibians, non-avian reptiles, and (non-human) mammals. As with birds, we document an inconsistent pattern across these other taxa. Within fish there was relatively broad support for an increase in plasma androgen levels in response to an experimental territorial challenge. That is, most fish showed a positive effect size with challenged males expressing higher testosterone and/or 11-ketotestosterone than controls, and the effect sizes were significantly positive in a good number of studies. However, the effect sizes in most mammals, all 4
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Fig. 3. Effect sizes of the change in testosterone during simulated territorial intrusion experiments in mammals (see Fig. 1 for details).
much more keenly responsive to the reproductive status of their mate and in which paternity is known. We would predict those truly monogamous males to be more responsive to female copulation solicitations than to male challenges. Further, the Challenge Hypothesis has not been tested in socially polygynous species such as those that exhibit lektype breeding systems. In those systems, males provide no paternal care of young, so there should be no trade-off between responding to a challenge and caring for young. Second, future studies should investigate male responses to interactions with females and these should be done across a wide variety of species. As we have recently proposed (Goymann et al., 2019), there is reason to believe that the opportunity for immediate reproductive success may be more important for mediating an androgen response than a challenge from another male that has only indirect possible reproductive benefits. Third, hormonal studies on the winner-and-loser effect suggest that androgens may be involved in mediating this effect (albeit the effects seem to substantially differ between taxa, e.g. Fuxjager et al., 2010; Fuxjager and Marler, 2010; Hirschenhauser et al., 2013; Oliveira et al., 2009). Currently, we lack an integration of the winner-and-loser paradigm with the Challenge Hypothesis [(see: Apfelbeck et al., 2011 for an attempt) and (Goymann et al., 2007; Kempenaers et al., 2008 for more detailed discussion)]. A rise in testosterone during male-male challenges has been suggested to increase the persistence of aggression and prepare the contestant for future encounters with other rivals, but experimental evidence for this, particularly in a field setting, is still limited [(Wingfield, 1994) (but see Goymann et al., 2015)]. In general, the incorporation of psychological studies (both human and rodent) into the eco-physiological realm would be productive. As our understanding of the neuroendocrine mechanisms and the context of aggression has been broadened (Eisenegger et al., 2011), their investigation in freeliving animals will further show if and how androgens mediate aggression. Most importantly, further conceptual contributions and experimental studies to elucidate the potential ecological and
male challenge as androgens suppress the former while they promote the latter. In such cases, responding to a conspecific challenge by elevating androgen levels would potentially have immediate negative effects on paternal care and thus fitness (e.g. Goymann and Dávila, 2017). However, for some animals including many fish, there is no trade-off between paternal care and responding to a conspecific territorial challenge. For fish, paternal care often means defending a nest site from competitors and predators as well as aerating the eggs. The same nest defense behavior also serves males to attract additional mates because females typically prefer to spawn with males that already have a nest with eggs (Coleman and Jones, 2011; Forsgren et al., 1996; Kahn et al., 2013). In those cases, there is no trade-off between mating effort and paternal care for androgens to mediate and thus androgens could have been co-opted to foster both kinds of behaviors. An increase in androgens could serve aggression and nest-tending at the same time with no associated costs in terms of parenting. Future studies should focus on a few distinct questions to try to understand variability in plasma androgen levels. First and foremost, a broader and more even distribution of sampling across the vertebrate classes is warranted. For example, we currently only have a single experimental study of an amphibian and yet amphibians offer a great variety of life-history traits and behaviors that are associated with androgens including paternal care, female mate choice, and male-male competition. Fish are another group with great variability in life-history traits associated with androgens. Focused studies on particular taxa, such as amphibians and fish that express a large variety in the degree of paternal care or mating system, are likely to provide important results from which broader conclusions can be made. Even within birds, the best studied group in terms of the Challenge Hypothesis, the majority of studies come from passerines with relatively similar life histories. The vast majority of passerines are socially monogamous but genetically polygynous. It could prove enlightening to test the Challenge Hypothesis in truly monogamous species in which males should be 5
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evolutionary benefits (and costs) of acute changes in androgen levels during social encounters are urgently needed.
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